Abstract
Citrus are economically important fruit crops to which infectious diseases like citrus canker caused by Xanthomonas citri subs. citri, citrus variegated chlorosis caused by Xylella fastidiosa, “huanglongbing” associated with the presence of Candidatus liberibacter species, anthracnose caused by Colletotrichum gloeosporioides and citrus black spot caused by Phyllosticta citricarpa, impose significant losses. Control measures involve chemical treatment of orchards but often, eradication of infected plants is unavoidable. To circumvent the environmental impacts of pesticides and the socio-economic impacts of eradication, innovative antimicrobial approaches like photodynamic inactivation are being tested. There is evidence of the susceptibility of Xanthomonas citri subs. citri and C. gloeosporioides to photodynamic damage. However, the realistic assessment of perspectives for widespread application of photodynamic inactivation in the control of citrus diseases, necessarily implies that other microorganisms are also considered. This review intends to provide a critical summary of the current state of research on photodynamic inactivation of citrus pathogens and to identify some of the current limitations to the widespread use of photodynamic treatments in citrus crops.
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References
Abdelfattah A, Cacciola SO, Mosca S, Zappia R, Schena L (2017) Analysis of the fungal diversity in citrus leaves with greasy spot disease symptoms. Microb Ecol 73(3):739–749. https://doi.org/10.1007/s00248-016-0874-x
Achor D, Etxeberria E, Wang N, Folimonova S, Chung K, Albrigo L (2010) Citrus affected with huanglongbing disease. Plant Pathol J 9:56–64
Aiello D, Carrieri R, Guarnaccia V, Vitale A, Lahoz E, Polizzi G (2015) Characterization and pathogenicity of Colletotrichum gloeosporioides and C. karstii causing preharvest disease on Citrus sinensis in Italy. J Phytopathol 163(3):168–177. https://doi.org/10.1111/jph.12299
Ajene IJ, Khamis FM, van Asch B, Pietersen G, Seid N, Rwomushana I, Ombura FL, Momanyi G, Finyange P, Rasowo BA (2020) Distribution of Candidatus Liberibacter species in Eastern Africa, and the first report of Candidatus Liberibacter asiaticus in Kenya. Sci Rep 10(1):1–10. https://doi.org/10.1038/s41598-020-60712-0
Alananbeh KM, BouQellah NA, Al Harbi MR, Ouf SA (2018) The efficacy of photosensitizers on mycelium growth, mycotoxin and enzyme activity of Alternaria spp. Jordan J Biol Sci 11(5):499–510
Almeida J, Tome JPC, Neves MGPMS, Tome AC, Cavaleiro JAS, Cunha A, Costa L, Faustino MAF, Almeida A (2014) Photodynamic inactivation of multidrug-resistant bacteria in hospital wastewaters: influence of residual antibiotics. Photoch Photobio Sci 13:626–633. https://doi.org/10.1039/C3PP50195G
Alves E, Marucci C, Lopes J, Leite B (2004) Leaf symptoms on plum, coffee and citrus and the relationship with the extent of xylem vessels colonized by Xylella fastidiosa. J Phytopathol 152(5):291–297. https://doi.org/10.1111/j.1439-0434.2004.00843.x
Alves G, Diniz A, Parra J (2014) Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. J Econ Entomol 107(2):691–696. https://doi.org/10.1603/EC13339
Alves E, Faustino MA, Neves MG, Cunha Â, Nadais H, Almeida A (2015) Potential applications of porphyrins in photodynamic inactivation beyond the medical scope. J Photoch Photobio C Photochem Rev 22:34–57. https://doi.org/10.1016/j.jphotochemrev.2014.09.003
Ambrosini V, Issawi M, Sol V, Riou C (2020) Photodynamic inactivation of Botrytis cinerea by an anionic porphyrin: an alternative pest management of grapevine. Sci Rep 10(1):1–12. https://doi.org/10.1038/s41598-020-74427-9
Avery’anov A, Lapikova V, Pasechnik T, Zakharenkova T, Pogosyan S, Baker C (2011) Suppression of cucurbit scab on cucumber leaves by photodynamic dyes. Crop Protect 30(7):925–930. https://doi.org/10.1016/j.cropro.2011.03.030
Bartolomeu M, Reis S, Fontes M, Neves MGP, Faustino MAF, Almeida A (2017) Photodynamic action against wastewater microorganisms and chemical pollutants: an effective approach with low environmental impact. Water 9(9):630. https://doi.org/10.3390/w9090630
Bassanezi RB, Montesino LH, Gimenes-Fernandes N, Yamamoto PT, Gottwald TR, Amorim L, Filho AB (2013) Efficacy of area-wide inoculum reduction and vector control on temporal progress of huanglongbing in young sweet orange plantings. Plant Dis 97(6):789–796. https://doi.org/10.1094/PDIS-03-12-0314-RE
Behlau F (2021) An overview of citrus canker in Brazil. Trop Plant Pathol 46(1):1–12. https://doi.org/10.1007/s40858-020-00377-2
Beirão S, Fernandes S, Coelho J, Faustino MA, Tomé JP, Neves MG, Tomé AC, Almeida A, Cunha A (2014) Photodynamic inactivation of bacterial and yeast biofilms with a cationic porphyrin. Photochem Photobiol 90(6):1387–1396. https://doi.org/10.1111/php.12331
Bi J, Dumenyo C, Hernandez-Martinez R, Cooksey D, Toscano N (2007) Effect of host plant xylem fluid on growth, aggregation, and attachment of Xylella fastidiosa. J Chem Ecol 33(3):493–500. https://doi.org/10.1007/s10886-006-9248-z
Bragg JD (1981) Inhibitory effects of light on ascospore germination of Pseudoarachniotus marginosporus. Mycologia 73(4):681–688. https://doi.org/10.1080/00275514.1981.12021395
Chignell CF, Bilskj P, Reszka KJ, Motten AG, Sik RH, Dahl TA (1994) Spectral and photochemical properties of curcumin. Photochem Photobiol 59(3):295–302. https://doi.org/10.1111/j.1751-1097.1994.tb05037.x
Coletta-Filho HD, Castillo AI, Laranjeira FF, de Andrade EC, Silva NT, de Souza AA, Bossi ME, Almeida RP, Lopes JR (2020) Citrus variegated chlorosis: an overview of 30 years of research and disease management. Trop Plant Pathol 45:175–191. https://doi.org/10.1007/s40858-020-00358-5
Correa TQ, Blanco KC, Garcia EB, Perez SML, Chianfrone DJ, Morais VS, Bagnato VS (2020) Effects of ultraviolet light and curcumin-mediated photodynamic inactivation on microbiological food safety: a study in meat and fruit. Photodiagn Photodyn 30:101678. https://doi.org/10.1016/j.pdpdt.2020.101678
Costa L, Carvalho CMB, Faustino MAF, Neves MG, Tomé JPC, Tomé AC, Cavaleiro JAS, Cunha Â, Almeida A (2010) Sewage bacteriophage inactivation by cationic porphyrins: influence of light parameters. Photoch Photobio Sci 9(8):1126–1133. https://doi.org/10.1039/C0PP00051E
Craig AP, Cunniffe NJ, Parry M, Laranjeira FF, Gilligan CA (2018) Grower and regulator conflict in management of the citrus disease Huanglongbing in Brazil: a modelling study. J Appl Ecol 55(4):1956–1965. https://doi.org/10.1111/1365-2664.13122
da Silva RN, Tomé AC, Tomé JPC, Neves MGPMS, Faustino MAF, Cavaleiro JAS, Oliveira A, Almeida A, Cunha  (2012) Photo-inactivation of Bacillus endospores: inter-specific variability of inactivation efficiency. Microbiol Immunol 56(10):692–699. https://doi.org/10.1111/j.1348-0421.2012.00493.x
Das A (2003) Citrus canker - a review. J Appl Hortic 5(1):52–60
de Menezes HD, Pereira AC, Brancini GTP, de Leão HC, Massola Júnior NS, Bachmann L, Wainwright M, Bastos JK, Braga GUL (2014a) Furocoumarins and coumarins photoinactivate Colletotrichum acutatum and Aspergillus nidulans fungi under solar radiation. J Photochem Photobiol B: Biol 131:74–83. https://doi.org/10.1016/j.jphotobiol.2014.01.008
de Menezes HD, Rodrigues GB, de Pádua TS, Massola NS, Bachmann L, Wainwright M, Braga GU (2014b) In vitro photodynamic inactivation of plant-pathogenic fungi Colletotrichum acutatum and Colletotrichum gloeosporioides with novel phenothiazinium photosensitizers. Appl Environ Microb 80(5):1623–1632. https://doi.org/10.1128/AEM.02788-13
de Menezes HD, Tonani L, Bachmann L, Wainwright M, Braga GÚL, von Zeska Kress MR (2016) Photodynamic treatment with phenothiazinium photosensitizers kills both ungerminated and germinated microconidia of the pathogenic fungi Fusarium oxysporum, Fusarium moniliforme and Fusarium solani. J Photochem Photobiol B: Biol 164:1–12. https://doi.org/10.1016/j.jphotobiol.2016.09.008
de Souza LM, Inada NM, Venturini FP, Carmona-Vargas CC, Pratavieira S, de Oliveira KT, Kurachi C, Bagnato VS (2019) Photolarvicidal effect of curcuminoids from Curcuma longa Linn. against Aedes aegypti larvae. J Asia-Pacif Entomol 22(1):151–158. https://doi.org/10.1016/j.aspen.2018.12.016
de Souza AA, Wang N, Coletta-Filho HD, Del Ponte EM (2020) Special issue on bacterial citrus diseases: part I. Trop Plant Pathol 45(3):163–165. https://doi.org/10.1007/s40858-020-00384-3
Del Campo R, Russi P, Mara P, Mara H, Peyrou M, De León IP, Gaggero C (2009) Xanthomonas axonopodis pv. citri enters the VBNC state after copper treatment and retains its virulence. FEMS Microbiol Lett 298(2):143–148. https://doi.org/10.1111/j.1574-6968.2009.01709.x
Dewdney MM, Schubert T, Estes M, Roberts P, Peres N (2010) Citrus black spot. Citrus Ind 91:19–20
Ding F, Duan Y, Paul C, Brlansky RH, Hartung JS (2015) Localization and distribution of ‘Candidatus Liberibacter asiaticus’ in citrus and periwinkle by direct tissue blot immuno assay with an anti-OmpA polyclonal antibody. PLoS ONE 10(5):e0123939. https://doi.org/10.1371/journal.pone.0123939
EU (2017) European Commission - A European One Health Action Plan against Antimicrobial Resistance (AMR).
EU (2019) European Commission - Commission Delegated Regulation (EU) 2019/1702 supplementing Regulation (EU) 2016/2031 of the European Parliament and of the Council by establishing the list of priority pests. Official Journal of the European Union L260/8.
FAO (2021) Citrus fruit-fresh and processed. Statistical bulletin 2020. In: Nations FaAOotU (ed) Statistical Bulletin. p 48
Fracarolli L, Rodrigues GB, Pereira AC, Massola Júnior NS, Silva-Junior GJ, Bachmann L, Wainwright M, Bastos JK, Braga GUL (2016) Inactivation of plant-pathogenic fungus Colletotrichum acutatum with natural plant-produced photosensitizers under solar radiation. J Photochem Photobiol B: Biol 162:402–411. https://doi.org/10.1016/j.jphotobiol.2016.07.009
Gabriel D, Gottwald TR, Lopes SA, Wulff NA (2020) Bacterial pathogens of citrus: citrus canker, citrus variegated chlorosis and Huanglongbing. In: Talon M, Caruso M, Gmitter FG (eds) The genus citrus. Woodhead Publishing, Sawston, pp 371–389. https://doi.org/10.1016/B978-0-12-812163-4.00018-8
Garcia M, David B, Sierra-Garcia IN, Faustino MAF, Alves A, Esteves AC, Cunha A (2021) Photodynamic inactivation of Lasiodiplodia theobromae: lighting the way towards an environmentally friendly phytosanitary treatment. Biol Lett 17(4):20200820. https://doi.org/10.1098/rsbl.2020.0820
Gholami D, Aminzadeh S, Alavi SM, Kazemipour N, Ghoroghi A, Emruzi Z (2018) Comparison of antibiotics and bacteriocins antibacterial activity on Xanthomonas citri subsp. citri. Fish Sci 17:162–178. https://doi.org/10.22092/ijfs.2018.115592
Glueck M, Hamminger C, Fefer M, Liu J, Plaetzer K (2019) Save the crop: photodynamic Inactivation of plant pathogens I: bacteria. Photoch Photobio Sci 18:1700. https://doi.org/10.1039/C9PP00128J
Gomes MC, Woranovicz-Barreira SM, Faustino MAF, Fernandes R, Neves MGPMS, Tome AC, Gomes NCM, Almeida A, Cavaleiro JAS, Cunha A, Tome JPC (2011) Photodynamic inactivation of Penicillium chrysogenum conidia by cationic porphyrins. Photoch Photobio Sci 10(11):1735–1743. https://doi.org/10.1039/C1PP05174A
Gonzales JC, Brancini GT, Rodrigues GB, Silva-Junior GJ, Bachmann L, Wainwright M, Braga GÚ (2017) Photodynamic inactivation of conidia of the fungus Colletotrichum abscissum on Citrus sinensis plants with methylene blue under solar radiation. J Photochem Photobiol B: Biol 176:54–61. https://doi.org/10.1016/j.jphotobiol.2017.09.008
Guarnaccia V, Crous PW (2018) Species of Diaporthe on Camellia and Citrus in the Azores Islands. Phytopathol Mediterr 57(2):307–319. https://doi.org/10.14601/Phytopathol_Mediterr-23254
Guarnaccia V, Gehrmann T, Silva-Junior GJ, Fourie PH, Haridas S, Vu D, Spatafora J, Martin FM, Robert V, Grigoriev IV (2019) Phyllosticta citricarpa and sister species of global importance to Citrus. Mol Plant Pathol 20(12):1619–1635. https://doi.org/10.1111/mpp.12861
Guillaumot D, Issawi M, Da Silva A, Leroy-Lhez S, Sol V, Riou C (2016) Synergistic enhancement of tolerance mechanisms in response to photoactivation of cationic tetra (N-methylpyridyl) porphyrins in tomato plantlets. J Photochem Photobiol B: Biol 156:69–78. https://doi.org/10.1016/j.jphotobiol.2016.01.015
Hall D, Richardson M (2013) Toxicity of insecticidal soaps to the Asian citrus psyllid and two of its natural enemies. J Appl Entomol 137(5):347–354. https://doi.org/10.1111/j.1439-0418.2012.01749.x
Hao W, Miles TD, Martin FN, Browne GT, Förster H, Adaskaveg JE (2018) Temporal occurrence and niche preferences of Phytophthora spp. causing brown rot of citrus in the Central Valley of California. Phytopathology 108(3):384–391. https://doi.org/10.1094/PHYTO-09-17-0315-R
Hu J, Jiang J, Wang N (2018) Control of citrus Huanglongbing via trunk injection of plant defense activators and antibiotics. Phytopathology 108(2):186–195. https://doi.org/10.1094/PHYTO-05-17-0175-R
Huang F, Fu Y, Nie D, Stewart JE, Peever TL, Li H (2015) Identification of a novel phylogenetic lineage of Alternaria alternata causing citrus brown spot in China. Fungal Biol 119(5):320–330. https://doi.org/10.1016/j.funbio.2014.09.006
Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol Plant-Microbe Interact 14(6):749–757. https://doi.org/10.1094/MPMI.2001.14.6.749
Jaouad M, Moinina A, Ezrari S, Lahlali R (2020) Key pests and diseases of citrus trees with emphasis on root rot diseases: an overview. Moroc J Agri Sci 1(3):149–160
Jesus V, Martins D, Branco T, Valério N, Neves MG, Faustino MA, Reis L, Barreal E, Gallego PP, Almeida A (2018) An insight into the photodynamic approach versus copper formulations in the control of Pseudomonas syringae pv. actinidiae in kiwi plants. Photoch Photobio Sci 17(2):180–191. https://doi.org/10.1039/C7PP00300E
Jiang L, Liu Y, Xu X, Su D, Zou H, Liu J, Yuan C, Huang M (2020) Inhibition of the citrus canker pathogen using a photosensitizer assisted by sunlight irradiation. Front Microbiol 11:571691–571691. https://doi.org/10.3389/fmicb.2020.571691
Khan MM, Reddy KV, Keshavayya J (2012) Synthesis, spectral, magnetic, thermal and antimicrobial studies on symmetrically substituted 2, 9, 16, 23-tetra-phenyliminophthalocyanine complexes. In: Bobbarala V (ed) A search for antibacterial agents. InTechOpen, Rijeka, pp 305–318
Kim B, Kim J, Kim H, Heo M (1997) Biological screening of 100 plant extracts for cosmetic use (II): anti-oxidative activity and free radical scavenging activity. Int J Cosmetic Sci 19(6):299–307. https://doi.org/10.1111/j.1467-2494.1997.tb00194.x
Kwiatkowski S, Knap B, Przystupski D, Saczko J, Kędzierska E, Knap-Czop K, Kotlińska J, Michel O, Kotowski K, Kulbacka J (2018) Photodynamic therapy–mechanisms, photosensitizers and combinations. Biomed Pharmacother 106:1098–1107. https://doi.org/10.1016/j.biopha.2018.07.049
La Torre A, Righi L, Iovino V, Battaglia V (2019) Evaluation of copper alternative products to control grape downy mildew in organic farming. J Plant Pathol 101(4):1005–1012. https://doi.org/10.1007/s42161-019-00330-6
Lacava P, Araújo W, Marcon J, Maccheroni W Jr, Azevedo JL (2004) Interaction between endophytic bacteria from citrus plants and the phytopathogenic bacteria Xylella fastidiosa, causal agent of citrus-variegated chlorosis. Lett Appl Microbiol 39(1):55–59. https://doi.org/10.1111/j.1472-765X.2004.01543.x
Lemos EGdM, Alves LMC, Campanharo JC (2003) Genomics-based design of defined growth media for the plant pathogen Xylella fastidiosa. FEMS Microbiol Lett 219(1):39–45. https://doi.org/10.1016/s0378-1097(02)01189-8
Lima WG, Spósito MB, Amorim L, Gonçalves FP, de Filho PAM (2011) Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. Eur J Plant Pathol 131(1):157–165. https://doi.org/10.1007/s10658-011-9795-1
Lima AR, Silva CM, Caires CS, Prado ED, Rocha LR, Cabrini I, Arruda EJ, Oliveira SL, Caires AR (2018) Evaluation of eosin-methylene blue as a photosensitizer for larval control of Aedes aegypti by a photodynamic process. Insects 9(3):109. https://doi.org/10.3390/insects9030109
Liu D, Gu W, Wang L (2021) Photodynamic inactivation and its application in food preservation. Crit Rev Food Sci. https://doi.org/10.1080/10408398.2021.1969892
Majiya H, Galstyan A (2020) Dye extract of calyces of Hibiscus sabdariffa has photodynamic antibacterial activity: a prospect for sunlight-driven fresh produce sanitation. Food Sci Nutr 8(7):3200–3211. https://doi.org/10.1002/fsn3.1580
Martins D, Mesquita MQ, Neves MG, Faustino MA, Reis L, Figueira E, Almeida A (2018) Photoinactivation of Pseudomonas syringae pv. actinidiae in kiwifruit plants by cationic porphyrins. Planta 248(2):409–421. https://doi.org/10.1007/s00425-018-2913-y
McEwen SA, Collignon PJ (2018) Antimicrobial resistance: a one health perspective. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.ARBA-0009-2017
Merfa MV, Pérez-López E, Naranjo E, Jain M, Gabriel DW, De La Fuente L (2019) Progress and obstacles in culturing ‘Candidatus Liberibacter asiaticus’, the bacterium associated with Huanglongbing. Phytopathology 109(7):1092–1101. https://doi.org/10.1094/PHYTO-02-19-0051-RVW
Michaeli A, Feitelson J (1994) Reactivity of singlet oxygen toward amino acids and peptides. Photochem Photobiol 59(3):284–289. https://doi.org/10.1111/j.1751-1097.1994.tb05035.x
Milanez JM, Parra JR, Custódio IA, Magri DC, Cera C, Lopes JR (2003) Feeding and survival of citrus sharpshooters (Hemiptera: Cicadellidae) on host plants. Florida Entomol 86(2):154–157. https://doi.org/10.1653/0015-4040(2003)086[0154:FASOCS]2.0.CO;2
Monzó C, Stansly PA (2020) Economic value of conservation biological control for management of the Asian citrus psyllid, vector of citrus Huanglongbing disease. Pest Manage Sci 76(5):1691–1698. https://doi.org/10.1002/ps.5691
Mukai K, Daifuku K, Okabe K, Tanigaki T, Inoue K (1991) Structure-activity relationship in the quenching reaction of singlet oxygen by tocopherol (vitamin E) derivatives and related phenols. Finding of linear correlation between the rates of quenching of singlet oxygen and scavenging of peroxyl and phenoxyl radicals in solution. J Org Chem 56(13):4188–4192. https://doi.org/10.1021/jo00013a021
Naranjo E, Merfa MV, Ferreira V, Jain M, Davis MJ, Bahar O, Gabriel DW, De La Fuente L (2019) Liberibacter crescens biofilm formation in vitro: establishment of a model system for pathogenic ‘Candidatus Liberibacter spp.’. Sci Rep 9(1):1–16. https://doi.org/10.1038/s41598-019-41495-5
Ndemueda A, Pereira I, Faustino M, Cunha  (2020) Photodynamic inactivation of the phytopathogenic bacterium Xanthomonas citri subsp. citri. Lett Appl Microbiol 71(4):420–427. https://doi.org/10.1111/lam.13350
Oliveira A, Almeida A, Carvalho CMB, Tomé JPC, Faustino MAF, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha A (2009) Porphyrin derivatives as photosensitizers for the inactivation of Bacillus cereus endospores. J Appl Microbiol 106(6):1986–1995. https://doi.org/10.1111/j.1365-2672.2009.04168.x
Peres N, Souza N, Peever T, Timmer L (2004) Benomyl sensitivity of isolates of Colletotrichum acutatum and C. gloeosporioides from citrus. Plant Dis 88(2):125–130. https://doi.org/10.1094/PDIS.2004.88.2.125
Peres NA, MacKenzie S, Peever T, Timmer L (2008) Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology 98(3):345–352. https://doi.org/10.1094/PHYTO-98-3-0345
Piccirillo G, Carrieri R, Polizzi G, Azzaro A, Lahoz E, Fernández-Ortuño D, Vitale A (2018) In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Sci Hortic 236:90–95. https://doi.org/10.1016/j.scienta.2018.03.044
Pimprikar GD, Norment BR, Heitz JR (1979) Toxicity of rose bengal to various instars of Culex pipiens quinquefasciatus and Aedes triseriatus. Environ Entomol 8(5):856–859. https://doi.org/10.1093/ee/8.5.856
Preuß A, Pfitzner M, Röder B (2019) Mosquito larvae control by photodynamic inactivation of their intestinal flora–a proof of principal study on Chaoborus sp. Photoch Photobio Sci 18(10):2374–2380. https://doi.org/10.1039/C9PP00156E
Ramos AP, Talhinhas P, Sreenivasaprasad S, Oliveira H (2016) Characterization of Colletotrichum gloeosporioides, as the main causal agent of citrus anthracnose, and C. karstii as species preferentially associated with lemon twig dieback in Portugal. Phytoparasitica 44(4):549–561. https://doi.org/10.1007/s12600-016-0537-y
Ramos-González PL, Chabi-Jesus C, Guerra-Peraza O, Tassi AD, Kitajima EW, Harakava R, Salaroli RB, Freitas-Astúa J (2017) Citrus leprosis virus N: a new dichorhavirus causing citrus leprosis disease. Phytopathology 107(8):963–976. https://doi.org/10.1094/PHYTO-02-17-0042-R
Robinson J (1983) Photodynamic insecticides: a review of studies on photosensitizing dyes as insect control agents, their practical application, hazards, and residues. Residue Rev 88:69–100. https://doi.org/10.1007/978-1-4612-5569-7_2
Rodrigues CM, Takita MA, Coletta-Filho HD, Olivato JC, Caserta R, Machado MA, De Souza AA (2008) Copper resistance of biofilm cells of the plant pathogen Xylella fastidiosa. Appl Microbiol Biot 77(5):1145–1157. https://doi.org/10.1007/s00253-007-1232-1
Salim HAM, Idrees SA, Rashid RA, Mohammed AA, Simo SM, Khalo (2018) IS photo-catalytic degradation of toluidine blue dye in aqueous medium under fluorescent light. In: 2018 International Conference on Advanced Science and Engineering (ICOASE). IEEE, pp 384–388. https://doi.org/10.1109/ICOASE.2018.8548935
Sechler A, Schuenzel EL, Cooke P, Donnua S, Thaveechai N, Postnikova E, Stone AL, Schneider WL, Damsteegt VD, Schaad NW (2009) Cultivation of ‘Candidatus Liberibacter asiaticus’, ‘Ca. L. africanus’, and ‘Ca. L. americanus’ associated with Huanglongbing. Phytopathology 99(5):480–486. https://doi.org/10.1094/phyto-99-5-0480
Shanmugam G, Jeon J, Hyun J-W (2020) Draft genome sequences of Elsinoë fawcettii and Elsinoë australis causing scab diseases on citrus. Mol Plant-Microbe Interact 33(2):135–137. https://doi.org/10.1094/MPMI-06-19-0169-A
Shiao S-H, Weng S-C, Luan L, Vicente MdGH, Jiang X-J, Ng DK, Kolli BK, Chang KP (2019) Novel phthalocyanines activated by dim light for mosquito larva-and cell-inactivation with inference for their potential as broad-spectrum photodynamic insecticides. PLoS ONE 14(5):e0217355. https://doi.org/10.1371/journal.pone.0217355
Silva-Stenico M, Pacheco F, Pereira-Filho E, Rodrigues J, Souza A, Etchegaray A, Gomes J, Tsai S (2009) Nutritional deficiency in citrus with symptoms of citrus variegated chlorosis disease. Braz J Biol 69:859–864. https://doi.org/10.1590/S1519-69842009000400013
Singerman A, Burani-Arouca M, Futch SH (2018) The profitability of new citrus plantings in Florida in the era of huanglongbing. Hort Sci 53(11):1655–1663. https://doi.org/10.21273/HORTSCI13410-18
Song BH, Lee DH, Kim BC, Ku SH, Park EJ, Kwon IH, Kim KH, Kim KJ (2014) Photodynamic therapy using chlorophyll-a in the treatment of acne vulgaris: a randomized, single-blind, split-face study. J Am Acad Dermatol 71(4):764–771. https://doi.org/10.1016/j.jaad.2014.05.047
Song R, Feng Y, Wang D, Xu Z, Li Z, Shao X (2017) Phytoalexin phenalenone derivatives inactivate mosquito larvae and root-knot nematode as type-II photosensitizer. Sci Rep 7(1):1–9. https://doi.org/10.1038/srep42058
Tang J, Tang G, Niu J, Yang J, Zhou Z, Gao Y, Chen X, Tian Y, Li Y, Li J (2021) Preparation of a porphyrin metal–organic framework with desirable photodynamic antimicrobial activity for sustainable plant disease management. J Agric Food Chem 69(8):2382–2391. https://doi.org/10.1021/acs.jafc.0c06487
Tansey JA, Vanaclocha P, Monzo C, Jones M, Stansly PA (2017) Costs and benefits of insecticide and foliar nutrient applications to huanglongbing-infected citrus trees. Pest Manage Sci 73(5):904–916. https://doi.org/10.1002/ps.4362
Tavares A, Carvalho CMB, Faustino MA, Neves MGPMS, Tomé JPC, Tomé AC, Cavaleiro JAS, Cunha Â, Gomes NCM, Alves E, Almeida A (2010) Antimicrobial photodynamic therapy: study of bacterial recovery viability and potential development of resistance after treatment. Mar Drugs 8(1):91–105. https://doi.org/10.3390/md8010091
Tavares A, Dias SR, Carvalho CM, Faustino MA, Tomé JP, Neves MG, Tome AC, Cavaleiro JA, Cunha Â, Gomes NC (2011) Mechanisms of photodynamic inactivation of a Gram-negative recombinant bioluminescent bacterium by cationic porphyrins. Photoch Photobio Sci 10(10):1659–1669. https://doi.org/10.1039/C1PP05097D
Tiwari S, Mann RS, Rogers ME, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manage Sci 67(10):1258–1268. https://doi.org/10.1002/ps.2181
Tran NT, Miles AK, Dietzgen RG, Shuey TA, Mudge SR, Papacek D, Chandra KA, Drenth A (2020) Inoculum dynamics and infection of citrus fruit by Phyllosticta citricarpa. Phytopathology 110(10):1680–1692. https://doi.org/10.1094/PHYTO-02-20-0047-R
USDA (2021) Citrus diseases. https://www.aphis.usda.gov/aphis/ourfocus/planthealth/plant-pest-and-disease-programs/pests-and-diseases/citrus. Accessed 13 Oct 2021
Vandresen CC, Goncalves AG, Ducatti DRB, Murakami FS, Noseda MD, Duarte MER, Barreira SMW (2016) In vitro photodynamic inactivation of conidia of the phytopathogenic fungus Colletotrichum graminicola with cationic porphyrins. Photoch Photobio Sci 15(5):673–681
Vega B, Dewdney MM (2014) Distribution of QoI resistance in populations of tangerine-infecting Alternaria alternata in Florida. Plant Dis 98(1):67–76. https://doi.org/10.1094/PDIS-04-13-0449-RE
Wagstaff DJ (1991) Dietary exposure to furocoumarins. Regul Toxicol Pharmacol 14(3):261–272. https://doi.org/10.1016/0273-2300(91)90029-U
Wang Z, Yin Y, Hu H, Yuan Q, Peng G, Xia Y (2006) Development and application of molecular-based diagnosis for ‘Candidatus Liberibacter asiaticus’, the causal pathogen of citrus huanglongbing. Plant Pathol 55(5):630–638. https://doi.org/10.1111/j.1365-3059.2006.01438.x
Yang J, Zhang B-W, Lin L-N, Zan X-L, Zhang G-C, Chen G-S, Ji J-Y, Ma W-H (2020) Key factors affecting photoactivated fungicidal activity of sodium pheophorbide a against Pestalotiopsis neglecta. Pestic Biochem Phys 167:104584. https://doi.org/10.1016/j.pestbp.2020.104584
Younis M, Hussein A, Aboelela H, Rashed G (2021) The potential role of photosensitizers in fight against mosquitoes: phototoxicity of Rose Bengal against Culex Pipiens larvae. Benha Medl J 38:1–10
Zhang Y, Dai T, Wang M, Vecchio D, Chiang LY, Hamblin MR (2015) Potentiation of antimicrobial photodynamic inactivation mediated by a cationic fullerene by added iodide: in vitro and in vivo studies. Nanomedicine 10(4):603–614. https://doi.org/10.2217/nnm.14.131
Zhang G, Yang J, Hu C, Zhang X, Li X, Gao S, Ouyang X, Ma N, Wei H (2019) Green synthesis of Chlorin e6 and tests of its photosensitive bactericidal activities. J Forestry Res 30(6):2349–2356. https://doi.org/10.1007/s11676-018-0756-9
Zhang X, Wu J, Xu C, Lu N, Gao Y, Xue Y, Li Z, Xue C, Tang Q (2020) Inactivation of microbes on fruit surfaces using photodynamic therapy and its influence on the postharvest shelf-life of fruits. Food Sci Technol Int 26(8):696–705. https://doi.org/10.1177/1082013220921330
Funding
This work was supported by project Rhizomis (PTDC/BIA-MIC/29736/2017) financed by Fundação para a Ciência e Tecnologia (FCT) through the Regional Operational Program of the Center (02/SAICT/2017) with FEDER funds (European Regional Development Fund, FNR and OE), and by the Research Units CESAM (UIDP/50017/2020 + UIDB/50017/2020), QOPNA (FCT UID/QUI/00062/2019), LAQV-REQUIMTE (UIDB/50006/2020), CICECO (UIDB/50011/2020 and UIDP/50011/2020) and iBiMED (UID/BIM/04501/2013). RNS acknowledges the support of project pAGE: (CENTRO-01-0145-FEDER-000003).
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JMRF, RNS and AC conceived the manuscript and defined the objectives. JF, AC and INSG provided the biological insight to the document and RNS, SG and AMSS contributed with expertise in organic chemistry. All authors revised and corrected the manuscript, and approved the final version.
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Ferreira, J.R.M., Sierra-Garcia, I.N., Guieu, S. et al. Photodynamic control of citrus crop diseases. World J Microbiol Biotechnol 37, 199 (2021). https://doi.org/10.1007/s11274-021-03171-7
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DOI: https://doi.org/10.1007/s11274-021-03171-7